Swirling Instability Mediated by Elastic and Hydrodynamic Couplings in Cytoplasmic Streaming

Cytoplasmic streaming is driven by molecular motors that move along the cytoskeleton and entrain the surrounding fluid. In certain cell types, the direction of cytoplasmic streaming is not predefined but rather stochastic. For example, in meiotic cytoplasmic streaming of zygotes, the direction of the swirl reverses over time [Kimura , ]. While a mean-field theory explained the reversal, the structure of flows in three-dimensional space and the mechanical role of the endoplasmic reticulum (ER) remains unknown. To test the hypothesis that the elastic ER bonds and hydrodynamic interactions between microtubules mediate the orientational order of microtubules, leading to directional cytoplasmic streaming, we computationally investigated fluid-structure interactions in cytoplasmic flow, ER networks, and microtubule structures in the presence of microtubule dynamic instability. The results indicate that the occasionally reversing swirls emerge within a certain range of ER elasticity, and our experimental measurements of the ER elasticity agree with the numerical predictions. Mass transport analysis further demonstrates that the reversing swirls are suitable for intracellular particle mixing. These findings illustrate the delicate balance of meiotic cytoplasmic streaming and provide insights into the physiology of the embryogenesis.